47

Changes in Abalone and Sea Urchin Populations
in Rocky Reef Ecosystems on the Sanriku Coast
Damaged by the Massive Tsunami andOther Environmental Changes Associated with
the Great East Japan Earthquake in 2011
Tomohiko KAWAMURA1*, Hideki TAKAMI2, Jun HAYAKAWA1, Nam-Il WON1,3,
Daisuke MURAOKA2,4 and Yutaka KURITA2
1International Coastal Research Center, Atmosphere and Ocean Research Institute, The University of Tokyo,2-106-1, Akahama, Otsuchi, Iwate 028-1102
5-1-5, Kashiwanoha, Kashiwa, Chiba, 277-8564 Japan
2
Tohoku National Fisheries Research Institute, Fisheries Research Agency,
3-27-5, Shinhama, Shiogama, Miyagi, 985-0001 Japan3
K-water Research Institute, Korea Water Resources Corporation,
Yuseonggu, Daejeon, 305-730 Korea
4
Miyako Laboratory, Tohoku National Fisheries Research Institute, Fisheries Research Agency,
4-9-1, Sakiyama, Miyako, Iwate, 027-0097 Japan*e-mail: kawamura@aori.u-tokyo.ac.jp

Abstract
Changes in populations of the abalone Haliotis discus hannai and sea urchin Strongylocentrotus nudus
following the tsunami and other events associated with the Great East Japan Earthquake which occurred on
March 11, 2011, are compared between two sites, Tomarihama on the Oshika Peninsula and Nagane in
Otsuchi Bay on the Sanriku Coast in northeastern Japan. As Tomarihama faces directly onto the Pacific Ocean,effects of the tsunami are likely to be heavier than at Nagane located near the mouth of Otsuchi Bay. At
Tomarihama, both adult and juvenile abalone were apparently affected by the tsunami disturbance, while at
Nagane in Otsuchi Bay, juvenile abalone <4 cm SL appeared to be more seriously affected by the tsunami thanadults. Sea urchin densities decreased considerably at both Tomarihama and Nagane, indicating that sea
urchins were more severely impacted by the event compared with abalone. The sea urchin density remained
low for two years after the event at Tomarihama, but recovered to almost the same level as before the tsunami
within six months from the event at Nagane. The results of the present study suggest that benthic organisms
which attach weakly to bottom substrates were more seriously impacted than strongly attached organisms.
Organisms inhabiting exposed areas suffer more effects than those inhabiting perennial kelp forests, where thecurrent velocity of the tsunami may be attenuated by the presence of the algal canopy. Although the damaged
populations have started recovering and/or adapting to the new environment, the speed and process of change
differ between the organisms and areas.
Key words: Haliotis discus hannai, marine rocky shore ecosystem, mega-earthquake,
Strongylocentrotus nudus, tsunami disturbance1. Introduction
Three years have passed since the mega-earthquake
known as the Great East Japan Earthquake occurred on
March 11, 2011. The effects of the massive tsunami andother environmental changes associated with the earthquake on marine ecosystems and the subsequent procGlobal Environmental Research
18/2014: 47-56
printed in Japanesses of change in the damaged ecosystems have been
continuously studied by many scientists, who provide
especially important information for the restoration anddevelopment of local fisheries in the disaster area. For
example, a major science project, the Tohoku Ecosystem-Associated Marine Sciences (TEAMS), funded by
the Ministry of Education, Culture, Sports, Science and©2014 AIRIES

48

T. KAWAMURA et al.

Technology, has been active since 2012. Institutes
belonging to the Fisheries Research Agency and local
governments in the disaster area have been intensively
studying the effects of the tsunami and other associatedevents following the earthquake on fishery resources andtheir habitats, mainly funded by the Ministry of Agriculture, Forestry, and Fisheries. These studies are also
scientifically important for elucidating how marine
ecosystems respond and change following such large
disturbances.
Although further intensive long-term studies areneeded to follow the recovery processes of various different marine ecosystems from such large and sudden
impacts by the tsunami and earthquake, we have now
begun to understand what happened and is happening inmarine ecosystems on the Sanriku and Joban coasts.
Effects of the tsunami are likely to vary considerably
based on location, local profile of the seafloor, and shapeof the coastline, even in a bay. Different ecosystems anddifferent organisms appear to receive different impacts.
In our previous paper, the impacts of the tsunami on
populations of the abalone Haliotis discus hannai and sea
urchin Strongylocentrotus nudus at Tomarihama on theeast coast of the Oshika Peninsula in Miyagi Prefectureon the southern Sanriku Coast were reported by comparing the data between the period before (from 29 July2010 to 9 February 2011) and after (8 June 2011) the
event (Takami et al., 2013). Both the abalone and sea
urchin are economically important fishery resources, andalso play important roles in the food web of the rocky
shore ecosystem (Won et al., 2011). The east side of the
Oshika Peninsula is the nearest coast from the epicenterof the earthquake, and as it happens, we have regularly
carried out quantitative surveys on the populations of theabalone and sea urchin, as well as other benthic animals
and macro-algae there, both before and after the tsunami.
Another continuous regular survey on the same
abalone and sea urchin species has been carried out on
the rocky reef at Nagane near the mouth of Otsuchi Bay
in Iwate on the Sanriku Coast, before and after thetsunami. Otsuchi Bay has been one of the major fields fortsunami and earthquake related marine ecological studies,as the International Coastal Research Centre (ICRC) of
the University of Tokyo’s Atmosphere and Ocean
Research Institute is located on the northern coast of thebay. Since the ICRC has been there for more than 40
years, many oceanographic and marine biological studies
have been carried out in and around Otsuchi Bay, andthus scientific information about marine ecosystems inthe bay before the earthquake has been accumulated. The
Coastal Ecosystem Restoration laboratory, to which thefirst author T. Kawamura and the third author J.
Hayakawa belong, was established by the ICRC in April
2012, a year after the earthquake, to lead studies on thetsunami and earthquake.
In this paper, changes in the abalone and sea urchin
populations since the tsunami and other events associatedwith the earthquake are compared between the two sites,
Tomarihama on the Oshika Peninsula and Nagane in

Otsuchi Bay. The effects of the tsunami and other environmental changes following the mega-earthquake on
benthic organisms in the rocky reef ecosystems of theSanriku Coast are summarized.

2. Materials and Methods
Quantitative surveys were conducted in the subtidal
rocky reefs at the two sites on the Sanriku Coast,
Tomarihama (38° 21’ N, 141° 32’ E) on the Oshika
Peninsula and Nagane (39° 21’ N, 141° 57’ E) in Otsuchi
Bay (Fig. 1). Tomarihama is 130 km west of the earthquake’s epicenter, and is a small open rocky shore facing
directly to the Pacific Ocean (Fig. 1), while Nagane islocated on the north coast near the mouth of Otsuchi Bay(Fig. 1), 160 km northwest of the earthquake’s epicenter.
In the subtidal area at Tomarihama, a clear algal
zonation mainly composed of three different macro-algal
communities had been continuously observed throughout
the year before March 2011: kelp beds (KB) dominatedby a perennial brown macroalga Eisenia bicyclis at 2 to
4 m depth, algal turf (AT) dominated by relatively small
red algae Gelidium elegans and/or Pterocladiella
capillacea at 4 to 5 m depth, and a crustose coralline algal
area (CCA) dominated by Lithophyllum yessoense at 5 to
8 m depth.
Likewise, in the subtidal area at Nagane in Otsuchi
Bay, a clear algal zonation of KB at 2 to 6 m depth and
CCA at 7 to 12 m depth, had been observed before March
2011. The KB was, however, dominated by a different
species of annual brown macro-alga, Saccharina
japonica var. religiosa. This kelp species starts growing
between April and May and forms dense communities on
rocky reefs, but dies back and is swept away from
October to November, with only the holdfast part remaining . Therefore, a clear algal zonation can be seen only
between April and November. The CCA was dominatedby Lithophyllum yessoense the same species as atTomarihama. Algal turf dominated by small red algae
was found in and around the kelp forest, but did not forma clear independent AT zonation at Nagane.
All fisheries were closed at both study sites after theearthquake, but the abalone fisheries were restarted in
November 2012 both in Otsuchi Bay and at Tomarihama.
The abalone H. discus hannai and sea urchin S. nudus
were quantitatively collected by scuba divers using
quadrats before and after the events at Tomarihama,
Oshika Peninsula (11 times for abalone: August andOctober 2009, July and November 2010, February, June,
August and December 2011, March and November 2012,
and March 2013, and eight times for sea urchin: June,
July and November 2010, June, August and December
2011, November 2012, and March 2013) and at Nagane
in Otsuchi Bay (11 times for abalone: September andDecember 2009, June, August and October 2010, July,
September and December 2011, March, June andOctober 2012, and ten times for sea urchin: December
2009, August and October 2010, July, September andDecember 2011, March, June and October 2012, andChanges in Abalone and Sea Urchin Populations Damaged by the Tsunami

49

Fig. 1 Location of the two study sites, Tomarihama on Oshika Peninsula and Nagane in Otsuchi Bay, andthe epicenter of the Great East Japan Earthquake.

March 2013). All of the surveys were conducted in themorning. Quadrats of 2 m × 2 m and 1 m × 1 m were used
for abalone and sea urchins, respectively, but 2 m × 2 m
for both abalone and sea urchins in June 2011 at
Tomarihama, and in July 2011 at Nagane, because of
their low densities. In each algal community (KB, AT,
and CCA), three (at Tomarihama) or four (at Nagane)
replicate quadrats were haphazardly located, and all
abalone and sea urchins in the quadrats were collected byhand and placed in mesh bags before being transported to
the laboratory of the Tohoku National Fisheries ResearchInstitute in Shiogama, Miyagi Pref. for the Tomarihama
survey, and that of the ICRC in Otsuchi, Iwate for the
Nagane survey, respectively. The shell length (SL) of
abalone and test diameter (TD) of sea urchins were
measured to the nearest 1 mm with calipers.
The relative abundance of young-of-the-year (YOY)abalone (< 17 mm SL) expressed as catch per unit effort(CPUE), accounting for the number of collected juveniles per searching time in hours, was measured andcompared between the period before (February 2011) andafter the tsunami (June 2011) at Tomarihama (Takami
et al., 2013). In the present study, the CPUE of juvenile
abalone (<50 mm SL) was monitored and compared
between the period before (October and December 2010)
and after the event (July 2011) at Nagane in Otsuchi Bay
by the same method as at Tomarihama, as follows.

Because the densities of YOY abalone at Nagane weremuch smaller than those at Tomarihama, 1-2-year-old
juveniles as well as YOY abalone were included for thisstudy. Since the distribution of juvenile abalone was too
cryptic and patchy to estimate their density by quadrat
sampling, the abundance of juveniles was monitored byintensive visual searching in their major habitat, CCA(Takami et al., 2012). In every survey, the same diversearched for juvenile abalone in every crevice and overhang, sometimes by overturning boulders and removing
large epibiota, recording how long each search took.
Juvenile abalone were carefully removed from substrata
and transferred to a sampling bottle with fine tweezers.
The SL of collected juvenile abalone was measured to thenearest 0.1 mm using a caliper or a video camera systemwith an image analyzer connected to a dissecting microscope in the laboratory.
Changes in abalone and sea urchin densities (individual number per m2) among dates of sampling were tested
by one-way analysis of variance (ANOVA) with Tukey’s
Honestly Significant Difference (HSD) test for each timeseries datum from the algal communities, as we focusedon the effects of the earthquake and tsunami. The data
were transformed (log n + 1) in order to achieve
homogeneity (Underwood, 1981). All statistical analyses
were carried out with JMP version 9.0.2 statisticalcomputer software (SAS Institute Inc., USA).

50

T. KAWAMURA et al.

3. Results

3.1.2 Nagane in Otsuchi Bay
Densities of adults and relatively large juveniles of
abalone sampled by quadrat survey varied significantly
between the algal communities, and the mean abalone
densities in the KB (0.4-1.8 individuals m-2) were always
higher than those in the CCA (0.0-0.6 individuals m-2)
during the survey (Fig. 4).
The abalone density in the KB showed no clear decrease between the period before October 2010 and after
the tsunami in July 2011, and no significant differenceswere found among the dates of sampling (ANOVA,
p > 0.05). After the event, the abalone density appeared
to increase gradually.
Also in the CCA, the abalone density did not decrease
between the periods before and after the event, and no
significant difference in density was observed among anyof the 11 surveys except for that of September 2009

Fig. 2 Temporal variation in densities of the abalone Haliotis
discus hannai collected from the kelp beds, algal turf andcrustose coralline algal area (CCA) at Tomarihama on
Oshika Peninsula. Bars denote standard error of the mean.
Character strings without any same letters indicate
significant differences (Tukey’s HSD test, P < 0.05). Blackline is drawn on 11 March 2011 when the Great East Japan
Earthquake and following massive tsunami occurred.
100

34 37

51

68 90

23 29 22

14

60

29

80

Shell Length(mm)Frequency (%)

3.1 Changes in the Abalone Population
3.1.1 Tomarihama on the Oshika Peninsula
Relatively large-sized adult and juvenile abalone
were collected mainly by quadrat survey. Before theevent, the mean abalone densities in the KB (2.6-5.2
individuals m-2) were always the highest among the threealgal communities, whereas the lowest mean abalone
densities of 0-0.6 individuals m-2 were observed in the
CCA (Fig. 2). The abalone densities had been on an increasing trend before the event in each algal community,and highest in February 2011.
In the KB, the density of abalone obtained by thequadrat survey in June 2011 after the tsunami had decreased considerably to 1.3 individuals m-2, which wassignificantly lower than that in February before the event(Tukey’s HSD test, p < 0.05), while no significant difference was observed among densities in the five surveys
before the event. The mean abalone densities remained at
the same level in the four surveys after the event, but
appeared to increase in November 2012, although nostatistically significant difference was detected in the fivesurveys after the event.
The mean densities in the AT and CCA had also
decreased in June 2011 (Fig. 2), but there were no significant differences in density between the five surveys
before and the first survey after the event (Tukey’s HSD
test, p > 0.05). Just as in the KB, the abalone densities inboth algal communities tended to recover after the event,although no significant differences in density were foundamong the six surveys after the tsunami (Tukey’s HSD
test, p > 0.05).
In June 2011, no abalone juveniles of two size classes< 20 mm SL and 20-40 mm SL, which had been continuously sampled before the event, were collected fromany of the three algal communities (Fig. 3). Individuals of
20-40 mm SL were found in five surveys after June 2011,
although small juveniles of < 20 mm SL were notcollected by the quadrat method at Tomarihama after thetsunami.

100≦
80‐100

60

60‐80
40‐60

40

20‐40
<20

20

0

2009

2010

2011

2012

2013

Fig. 3 Size composition in shell length of the abalone Haliotis
discus hannai collected at Tomarihama. Number on eachcolumn shows the number of collected individuals on thesampling date.

Fig. 4 Temporal variation in densities of the abalone Haliotis
discus hannai collected from the kelp beds and crustosecoralline algal area (CCA) at Nagane in Otsuchi Bay. Bars
denote standard error of the mean. Different letters in CCAline indicate significant differences (Tukey’s HSD test, P <0.05). Black line is drawn on 11 March 2011 when Great
East Japan Earthquake and following massive tsunami
occurred.

Changes in Abalone and Sea Urchin Populations Damaged by the Tsunami

3.2.2 Nagane in Otsuchi Bay
Before the event, the mean sea urchin densities in the
CCA (3.8-7.5 individuals m-2) were always higher thanthose in the KB (1.3-2.5 individuals m-2) (Fig. 9).

6

10

13

11 13

14

14

20

16

Shell Length
(mm)

80

100≦
80‐100

60

60‐80
40‐60
20‐40

40

<20

20

0

2010

2011

2012

Fig. 5 Size composition in shell length of the abalone Haliotis
discus hannai collected at Nagane. Number on eachcolumn shows the number of collected individuals on thesampling date.
8

Oct 2010
6

4

2

0

0 0 5 5 1010151520202525303035354040454550

8CPUE (inds diver‐1 h‐1)

3.2 Changes in the Sea Urchin Population
3.2.1 Tomarihama on the Oshika Peninsula
In the three surveys before the tsunami, the meandensities of sea urchin were always higher in the CCA(10-14 individuals m-2) and AT (5-19 individuals m-2)
than in the KB (1-3 individuals m-2) (Fig. 7).
In June 2011, three months after the tsunami, the sea
urchin density had decreased significantly in the CCA
and AT compared with densities sampled before the event(Tukey’s HSD test, p < 0.05). The sea urchin density in
the KB had also decreased clearly in June 2011 comparedwith the densities before the event, although no significant difference was detected in sea urchin density in the
KB among the dates of sampling (ANOVA, p > 0.05).
Sea urchin densities remained at a low level in all thealgal communities after the event (except the temporary
high mean density with a large standard error in August
2011 in the KB) until March 2013, the last survey in thepresent study (Fig. 7).
Due to the large decrease in the sea urchin density as aresult of the tsunami, the change in size composition of
the collected sea urchins was ambiguous, comparing
before and after the event (Fig. 8). However, no individuals smaller than 20 mm TD, which were usually
sampled at Tomarihama before the tsunami, were foundfrom any of the three algal communities in the five surveys after the event. In August and December 2011 (after
the tsunami) the frequencies of the 20-40 mm TD sizeclass were relatively low compared with the three surveys before the event, and no sea urchins smaller than
40 mm TD were collected in December 2011 (Fig. 8).

100

Frequency (%)(Tukey’s HSD test, p > 0.05), although statistically significant changes were detected in the density of abalone
among the dates of sampling (ANOVA, p < 0.05). No
abalone were found in the CCA in the four surveys after
the tsunami.
At Nagane, no clear change in the size composition
was observed between the periods before and after thetsunami. The frequency of juveniles collected by thequadrat survey was low even before the event, and no
individuals of < 20 mm SL size class were sampled fromthe KB or CCA in any of the three surveys before thetsunami (Fig. 5). While the low frequency of juveniles
remained after the event, the frequency of large adults of
the > 100 mm SL size class increased markedly compared to that before the event.
While the CPUE of juvenile abalone was almost thesame in October and December 2010, it decreased by
66% from December 2010 to July 2011 after the event(Fig. 6). No juvenile abalone smaller than 25 mm SL(except one individual of 7.0 mm SL) were found after
the event, although they were collected before thetsunami.

51

Dec 2010
6

4

2

0

0 0 5 5 1010151520202525303035354040454550

8

Jul 2011
6

4

2

0

0 0 5 5 1010151520202525303035354040454550

Shell length (mm)Fig. 6 Comparison of CPUE for the number of collectedjuvenile abalone Haliotis discus hannai per searchingtime in hours with size distribution among three surveys(October and December 2010, and July 2011) at Nagane.

In July 2011, the sea urchin densities in the CCA had
decreased from October 2010, but no significant difference in density was confirmed between the two dates ofsampling (Tukey’s HSD test, p > 0.05) (Fig. 9). The decrease in density in the KB was much smaller than in the
CCA, and no significant difference was found among anyof the dates of sampling (ANOVA, p > 0.05). After the
event, the sea urchin density in the CCA appeared toincrease gradually, including a temporary large increase

52

T. KAWAMURA et al.

Fig. 7 Temporal variation in densities of the sea urchin
Strongylocentrotus nudus collected from the kelp beds,
algal turf and crustose coralline algal area (CCA) at
Tomarihama on Oshika Peninsula. Bars denote standard
error of the mean. Different letters or numbers in eachline indicate significant differences (Tukey’s HSD test, P< 0.05). Black line is drawn on 11 March 2011 when the
Great East Japan Earthquake and following massive
tsunami occurred.

100

49 80

98

4 35

13

11

Fig. 9 Temporal variation in densities of the sea urchin
Strongylocentrotus nudus collected from the kelp beds
and crustose coralline algal area (CCA) at Nagane in
Otsuchi Bay. Bars denote standard error of the mean.
Different letters in each line indicate significant differences (Tukey’s HSD test, P < 0.05). Black line is drawn
on 11 March 2011 when the Great East Japan Earthquake
and following massive tsunami occurred.

26

20

100

32 40

59 29 41 71 40

44

80

80

Test Diameter(mm)

80‐100

60

60‐80
40‐60
20‐40

40

Frequency (%)

Test Diameter(mm)

Frequency (%)

23

100≦
80‐100

60

60‐80
40‐60
40

20‐40

<20

<20
20

20

0

0

2010

2011

2012

2013

2009

2010

2011

2012

2013

Fig. 8 Size composition in shell length of the sea urchin
Strongylocentrotus nudus collected at Tomarihama.
Number on each column shows the number of collectedindividuals on the sampling date.

Fig. 10 Size composition in shell length of the sea urchin
Strongylocentrotus nudus collected at Nagane. Number
on each column shows the number of collectedindividuals on the sampling date.

in March 2012. Although the sea urchin density in the
KB showed no clear increase after the tsunami, it maintained the equivalent level density as in the three surveys
before the event (Fig. 9).
Similarly to Tomarihama, the frequency of sea urchinsmaller than 40 mm TD became lower after the event(Fig. 10). No individuals smaller than 20 mm TD, whichwere found in the three surveys before the tsunami, werecollected from the two algal communities in the sevensurveys after the event. The frequency of the 20-40 mm
TD size class decreased after the tsunami, and sea urchinsof this size class were collected at Nagane only in two ofseven surveys after the event. From December 2011 to
October 2012, relatively large individuals (> 60 mm TD)
accounted for more than 90% of the collected sea urchins(Fig. 10).

4. Discussion
4.1 Changes in the Abalone Population
As we reported in our previous paper (Takami et al.,2013), both adult and juvenile abalone H. discus hannai
were apparently affected by the tsunami disturbance inthe rocky subtidal reefs at Tomarihama on the Oshika
Peninsula. The mean density of the abalone collected byquadrat survey in June 2011, three month following theevent, had decreased considerably in all three algal
communities (KB, AT and CCA) from that in February,a month before the event (Fig. 2). Many abalone
individuals appeared to have been dislodged andtransported offshore by the tsunami. In the six surveys
after the event until March 2013, the last survey for theabalone at Tomarihama in the present study, the densities
of abalone remained low level in the three algal com-

Changes in Abalone and Sea Urchin Populations Damaged by the Tsunami

munities (Fig. 2). Juvenile abalone smaller than ~4 cm
SL appeared to have been more seriously affected by thetsunami than adults, as suggested by the changes in thesize-frequency distributions (Fig. 3) and by the reductionin the CPUE of YOY abalone from February to June
2011 reported by Takami et al. (2013). Although themortality rate of YOY abalone is usually high when thecold Oyashio current extends south to the abalone habitat,
and the mean seawater temperature falls to below 5°C in
winter and early spring (Takami et al., 2008), the obvious
decrease in the CPUE of YOY abalone in 2011 at
Tomarihama was unlikely to be due to the low seawatertemperatures (Takami et al., 2013).
While at Nagane in Otsuchi Bay, no differences in
abalone density collected by quadrat method were foundin either the KB or CCA before or after the event (Fig. 4),
indicating that adults and large juveniles of abalone were
not heavily impacted by the tsunami. However, smaller
juvenile abalone were likely to have been reduced by thetsunami, as indicated by the reduction in the CPUE ofjuvenile abalone from December 2010 to July 2011
(Fig. 6). The relative abundance of juvenile abalone
indicated by the CPUE at both Tomarihama and Nagane
have been continuously surveyed following the tsunami
and other environmental changes associated with theearthquake, and will be reported in a discussion on
the recruitment processes at both sites (Takami et al., in
preparation).
The relatively weaker adhesion of juveniles to substrates compared to that of adults could partially explain
the more apparent impacts of the tsunami on smaller
individuals than larger abalone at both Tomarihama andNagane, as suggested by Naylor and McShane (2001) for
the New Zealand abalone H. iris against storm disturbances.
The abalone H. discus hannai changes its major
habitat as it grows (reviewed by Kawamura & Takami,2005). The swimming larvae selectively settle on the
CCA bed to metamorphose into crawling juveniles.
Juveniles live on the CCA bed for a year or more, thenmove to the AT as their transitional habitat, and to their
final habitat, the KB, when they grow to 4 - 5 cm SL, as
has been indicated by our observations for many years at
Tomarihama (Takami et al., 2012). Thus, adult abalone(> 5 cm) appeared to be found mainly in the Eisenia
bicyclis forest at KB while most juveniles were likely to
be on the CCA, outside of the kelp forest at Tomarihama
when the earthquake and tsunami attacked the area.
Consequently, juveniles inhabiting the CCA may havebeen more heavily damaged than the adults in the kelp
forest, as the velocity of the tsunami current may havebeen attenuated by the algal canopy (Whanpetch et al.,2010).
The major habitats of adult and juvenile abalone arealso the KB and CCA, respectively, at Nagane in Otsuchi
Bay. In early March 2011, when the earthquake andtsunami occurred, however, both adult and juvenile
abalone may have been living on exposed rocks at
Nagane, as the dominant kelp species Saccharina

53

religiosa at Nagane usually forms a dense community
only between April and October. Despite this, the adultabalone density in the KB without the kelp forest did notdecrease notably at Nagane, indicating that the impact of
the tsunami was much less at Nagane in Otsuchi Bay thanat Tomarihama on the Oshika Peninsula.
Densities of juvenile abalone, probably under three
years old at the time of the event, also appeared to decrease in many other areas affected by the tsunami (Goto& Ohmura, 2012; Nakaie & Takami, 2012). This implies
that recruits to the fishery resource (> ~9 cm SL) arelikely to decrease sharply two to four years after such
events, as the age at first capture of the abalone is four tofive years old (Sasaki, 1999). In addition, reseedings ofhatchery-reared juveniles have largely declined and may
not recover for several more years as most of thehatcheries producing H. discus hannai seeds were destroyed or seriously damaged by the tsunami. Stocks ofabalone for the fishery will largely decline in the next
several years.
4.2 Changes in the Sea Urchin Population
The mean densities of the sea urchin S. nudus largely
decreased in all three algal communities (KB, AT and
CCA) at Tomarihama from November 2010 (four months
before the event, Fig. 11A) to June 2011 (three months
after the event, Fig. 11B), although no statisticallysignificant differences were detected in the KB (Fig. 7).
At Nagane in Otsuchi Bay also, sea urchin densities in
the CCA appear to have decreased from October 2010 toJuly 2011, although no statistically significant difference
was detected probably due to the large variation of thedata during the whole survey period (Fig. 9). Thesechanges in sea urchin density indicate that the sea urchinswere more severely impacted by the event than theabalone, as even adult sea urchins decreased at Nagane in
Otsuchi Bay where the adult abalone density did notdecrease. This is probably because sea urchins adhere
less strongly to the substrate than abalone and are more
likely to be washed away (Kawamata, 2001). The
distribution pattern of sea urchins could also be a cause of
the marked decrease because most of the sea urchins
inhabited the AT and CCA at Tomarihama and the CCA at
Nagane, respectively, where the disturbance by themassive water movement was scarcely reduced by theeffects of the macroalgal forest. Although the swimminglarvae of the sea urchin selectively settle on the CCA bed
to metamorphose into crawling juveniles as the abalone
larvae do (Pearce & Scheibling, 1990; Rowley, 1989),
juvenile and adult sea urchins inhabit the CCA and AT
throughout their life and do not move into the KB. Thus
even adult sea urchins are likely to suffer more damage
than adult abalone living in the kelp forest.
At Nagane in Otsuchi Bay, the mean sea urchin density in the CCA apparently increased from July 2011 toMarch 2012 (Fig. 9). The sea urchin density then significantly decreased from March to June 2012 until it wasalmost the same level as before the tsunami. The densityof small-sized sea urchins, however, did not increase

54

T. KAWAMURA et al.

A

B

C

D

Fig.11 Underwater photographs of rocky seafloor at Tomarihama. (A) Bedrock covered with crustosecoralline algae in CCA with many sea urchins Strongylocentrotus nudus with a 2 m × 2 m
quadrat before the event (taken on 11 November 2010): from Takami et al. (2013); (B) CCA
after the event (taken on 8 June 2011). Large rocks were cracked and turned over on theseafloor, in consequence bare rock without any epibiota including crustose coralline algae were
exposed and no sea urchins were observed: from Takami et al. (2013); (C) Young recruits of anannual brown macroalga Undaria pinnatifida in CCA (taken on 8 June 2011): taken by Ryo
Sasaki; (D) Young recruits of a perennial brown macroalga Eisenia bicyclis in CCA (taken on
28 November 2012).

until October 2012 and thus the size distribution changed
after the event (Fig. 10). This kind of quick recovery indensity and change in size distribution of the sea urchin
after a catastrophic decrease due to the tsunami has been
observed in many places on the Sanriku Coast, although
there are no published data available at present. Largesized sea urchins might be able to survive better thanabalone and small-sized sea urchins after being dislodged
and transported away to deeper areas (Goto & Ohmura,2012). In addition, as large-sized sea urchins are likely tomove over a longer distance than small individuals andabalone, they could come back to shallow coastal areas,
their suitable habitat.
Meanwhile, at Tomarihama on the Oshika Peninsula,
the sea urchin densities in all three algal communities(KB, AT and CCA) were at low levels after the event,except the high mean density in the KB in August 2011,
and did not start recovering until March 2013 (Fig. 7).
The sea urchins at Tomarihama may have been washed
far away to deeper areas so that not even large-sized sea
urchins could have made it back.
4.3 Effects of the Earthquake and Tsunami on Rocky
Reef Ecosystems
As Tomarihama faces directly onto the Pacific Ocean,the effects of the tsunami are likely to have been heavier
than at Nagane, located near the mouth of Otsuchi Bay. In
fact, many large rocks had been cracked and rotated on

the rocky reef seafloor deeper than 5 m off Tomarihama(Fig. 11B; Takami et al., 2013), while no such kinds ofapparent impacts by the tsunami disturbance wereobserved on the rocky reef at Nagane in Otsuchi Bay. On
the rocky reefs at Nagane, a dense community (KB) of
the dominant kelp Saccharina religiosa was found and noapparent effect by the tsunami was observed in July 2011,
four months after the event. This may be because thisannual kelp species started forming a dense community
after the tsunami attacked the area. At Tomarihama,
however, the biomass of the perennial dominant kelp
species Eisenia bicyclis forming the community (KB)
throughout the year, was also not significantly decreasedby the tsunami (Takami et al., 2013). This indicates how
tough and flexible the macro-algae attached to rocky
reefs are against such kinds of large disturbances.
The benthic animals in coastal rocky reef ecosystems,
though, appear to have been affected variously by thetsunami at both Tomarihama and Nagane. The results ofthe present study suggest that benthic organisms attaching weakly to bottom substrates suffered more serious
impacts than strongly attached sessile organisms. Organisms inhabiting exposed areas are more likely to be
impacted than those living inside algal forests. Although
the damaged populations have started recovering and/or
adapting to the new environment, the speed and processof change differ among organisms. The changes in thecommunity structure of organisms resulting mainly from

Changes in Abalone and Sea Urchin Populations Damaged by the Tsunami

the tsunami, may affect the ecosystem and population ofeach organism for a long time.
The crustose coralline algae community is usually
maintained under high grazing pressures by herbivores
like sea urchins and gastropods, which prevent othercanopy-forming algae from growing on the crustosecoralline algal surface (Pinnegar et al., 2000; Scheibling
et al., 2009). After the earthquake and tsunami, new recruitments of juvenile macroalgae such as E. bicyclis andUndaria pinnatifida were observed on crustose coralline
algal surfaces in the CCA at Tomarihama (Figs. 11C, D;
Takami et al., 2013) and also at Nagane (the present
study), probably mainly due to the large-scale decrease in
the grazing pressure of sea urchins and other herbivores.
The expansion of both the E. bicyclis and the S. religiosa
community (KB) into the deeper CCA areas has been
seen at Tomarihama and Nagane, respectively (Muraoka
et al., unpublished), which may increase food sources for
adult abalone and sea urchins, but may decrease settlement areas for larvae and nursery areas for juveniles.
The water turbidity with sediment and subsequent
sedimentation on the rocky seafloor observed atTomarihama in June 2011 (Takami et al., 2013) were also
seen at Nagane in Otsuchi Bay in July 2011, and were
continuously observed for several months at both sites.
These were probably initially caused by the tsunami
disturbance and later by land subsidence triggered by theearthquake. The sediments may have been continuously
flowing into the coastal waters from the area flooded
after subsidence. Sediment on the surface of crustosecoralline algae may prevent larval abalone and sea
urchins from attaching and metamorphosing, as reported
for the small abalone H. diversicolor (Onitsuka et al.,2008). The settlement of macro-algal propagules wasreported to be prevented by sediment on the seafloor(Arakawa & Matsuike, 1992; Airoldi, 2003). The new
recruits of benthic animals including both the abalone H.
discus hannai and the sea urchin S. nudus as well as
macro-algae may be negatively affected by the increased
sedimentation on rocky reefs on the Sanriku Coast.
The impacts of the tsunami on coastal rocky reef
ecosystems appear to be relatively limited compared withsome other coastal ecosystems. Effects of the tsunami
have been much more severe and apparent on sandy
seafloors and mud flats. Many of the organisms living on
sandy or muddy seafloors were flushed away together
with the bottom substrates (Seike et al., 2013; Urabeet al., 2013). Large communities of seagrasses had
formed on the sandy bottom in the innermost part of
Otsuchi Bay before the event, but were heavily destroyedby the tsunami. Now the few remaining seagrass
individuals have started making seeds to recover theircommunities, but they will take at least several years to
be restored (Shoji, personal communication). Even inrocky reef ecosystems, however, the above-mentioned
direct and indirect effects of the earthquake and tsunami
may remain for a long time and could change food web
structures and interspecific interactions in the ecosystem.
Therefore, continuous long-term monitoring is important55

for elucidating the overall picture of effects of the earthquake and tsunami on marine ecosystems as well as tolearn how damaged populations of organisms respondand change following such large disturbances.
The coastal ecosystems and organisms inhabiting
them that were damaged by the earthquake and tsunami
may face further large-scale disturbances from humanactivities in relation to the restoration processes in thedisaster area, such as the reconstruction of fishing ports
and seawalls. The resumption of fisheries may also havemore negative impacts on damaged populations of thetarget species. Any human activities should be carefully
conducted following scientific advice, to minimize further negative effects on the damaged ecosystems, and toconserve healthy coastal ecosystems and subsequent
sustainable fisheries in the future.

Acknowledgements
We thank Ryo Sasaki for his useful comments andassistance in the field. This research was supported by theDevelopment Projects for Application in Promoting New
Policy of Agriculture Forestry and Fisheries Japan (grantNo. 2024), Tohoku Ecosystem-Associated Marine
Sciences and the Coastal Ecosystem Complex of the
Ministry of Education, Culture, Sports, Science andTechnology Japan.
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Tomohiko KAWAMURA
Tomohiko KAWAMURA is director of International
Coastal Research Center (ICRC), a branch of the
University of Tokyo’s Atmosphere and Ocean
Research Institute. The ICRC is located in
Otsuchi, Iwate, and was directly attacked andheavily damaged by the earthquake and tsunami
in March 2011. Besides being director of theinstitute, he works as a professor at a laboratory newly established in 2012
named “Coastal Ecosystem Restoration” at the ICRC, leading studies inrelation to the effects of the earthquake and tsunami events on coastal
ecosystems and organisms, and managing a major research project“Tohoku Ecosystem-Associated Marine Sciences,” based on his longexperience in ecological studies of marine benthic animals.

Hideki TAKAMI
Hideki TAKAMI is a senior scientist of the Coastal
Fisheries Resources Group, Stock Enhancement
and Aquaculture Division, Tohoku National
Fisheries Research Institute, Fisheries Research
Agency, Japan. He is a marine biologist focusing
on the ecology of fishery species associated withrocky shore ecosystems. He is currently involved
in some research projects related to the massive tsunami in March 2011,
e.g., projects studying the processes of recovery of destroyed ecosystems
and animal populations, and sustainable ways to manage resources of thedamaged populations.

Jun HAYAKAWA
Jun HAYAKAWA is an assistant professor at theInternational Coastal Research Center, the University of Tokyo, Japan. He received his Doctor of
Agriculture from the University of Tokyo in 2010.
His research has focused on the ecology ofbenthic animals and the interaction between
benthic and algal communities.

Nam-Il WON
Nam-Il WON received his B.S. and M.S. degrees
in Oceanography from Seoul National University
in Seoul, South Korea. He received his Ph.D. in
Aquatic Bioscience from the University of Tokyo,
Japan. After his work as a project researcher from2007 to 2011 at the Atmosphere and Ocean
Research Institute, he returned to South Korea toserve as a research professor at Korea University, Seoul. Since 2012, hehas been working as a principal researcher at the K-water Institute, Korea
Water Resources Corporation in Daejeon. His present work focuses on
examining the effects of freshwater on coastal ecosystems.

Daisuke MURAOKA
Daisuke MURAOKA is a group leader at the
Tohoku National Fisheries Research Institute(TNFRI), Fisheries Research Agency, Japan,
working in the Coastal Ecosystems Group,
Research Center for Coastal Fisheries andAquaculture. His fields of research include
seagrass and kelp forest ecosystems, with a focus
on the relationship between seaweeds and herbivores. He received his
B.S., M.S. and Ph.D. from Hokkaido University and has been working in
his current position since December 2013.

Yutaka KURITA
Yutaka KURITA is head scientist of the Coastal
Fisheries Resources Group, Stock Enhancement
and Aquaculture Division, Tohoku National
Fisheries Research Institute, Fisheries Research
Agency, Japan. He is a biologist studying life
histories, especially the reproductive traits, ofresource fishes. Recently, he has been involved insome research projects related to the massive tsunami and nuclear power
plant accident in March 2011, e.g., projects studying the process ofrecovery of destroyed ecosystems and animal populations, and themechanisms of temporal changes in radioactive cesium in resource fishes.

(Received 4 April 2014, Accepted 2 July 2014)